REVIEW

Minimally invasive oesophagectomy: current status and futuredirection

Nick Butler • Stuart Collins • Breda Memon •

Muhammed Ashraf Memon

Received: 24 February 2010 / Accepted: 26 July 2010

� Springer Science+Business Media, LLC 2011

Abstract

Background Oesophagectomy is one of the most chal-

lenging surgeries. Potential for morbidity and mortality is

high. Minimally invasive techniques have been introduced

in an attempt to reduce postoperative complications and

recovery times. Debate continues over whether these

techniques are beneficial to morbidity and whether onco-

logical resection is compromised. This review article will

analyse the different techniques employed in minimally

invasive oesophagectomy (MIO) and critically evaluate

commonly reported outcome measures from the available

literature.

Methods Medline, Embase, Science Citation Index,

Current Contents, and PubMed databases were used to

search English language articles published on MIO. Thirty-

one articles underwent thorough analysis and the data were

tabulated where appropriate. To date, only level III evi-

dence exists. Where appropriate, comparisons are made

with a meta-analysis on open oesophagectomy.

Results Positive aspects of MIO include at least compa-

rable postoperative recovery data and oncological resection

measures to open surgery. Intensive care unit requirements

are lower, as is duration of inpatient stay. Respiratory

morbidity varies. Negative aspects include increased

technical skill of the surgeon and increased equipment

requirements, increased operative time and limitation with

respect to local advancement of cancer. With increasing

individual experience, improvements in outcome measures

and the amenability of this approach to increasing neo-

plastic advancement has been shown.

Conclusion MIO has outcome measures at least as com-

parable to open oesophagectomy in the setting of benign

and nonlocally advanced cancer. Transthoracic oesophag-

ectomy provides superior exposure to the thoracic

oesophagus compared to the transhiatal approach and is

currently preferred. No multicentre randomised controlled

trials exist or are likely to come into fruition. As with all

surgery, careful patient selection is required for optimal

results from MIO.

Keywords Oesophagectomy � Laparoscopy �Oesophageal cancer � Retrospective studies � Prospective

studies � Comparative studies � Patient outcome �Intraoperative complications � Postoperative

complications � Hospitalisation � Human

Surgical resection and replacement of the neoplastic

oesophagus remains the definite therapeutic mode in order

to achieve cure. Other indications for operative interven-

tion include Barrett’s oesophagus with high-grade dyspla-

sia and benign disease refractory to medical or endoscopic

treatment. Irrespective of aetiology, oesophagectomy has

long been respected as one of the most challenging

N. Butler � S. Collins � B. Memon � M. A. Memon (&)

Department of Surgery, Ipswich Hospital, Chelmsford Avenue,

Ipswich, QLD, Australia

e-mail: mmemon@yahoo.com

M. A. Memon

Department of Surgery, University of Queensland, Brisbane,

QLD, Australia

M. A. Memon

Faculty of Health Sciences and Medicine, Bond University,

Gold Coast, QLD, Australia

M. A. Memon

Faculty of Health and Social Sciences, Bolton University,

Bolton, Lancashire, UK

123

Surg Endosc

DOI 10.1007/s00464-010-1511-2

surgeries, with the combination of oesophageal anatomy

and patient demographics giving a high potential for both

morbidity and mortality. Recently, larger centres have

introduced minimally invasive techniques in an attempt to

reduce postoperative complications and recovery times.

Since the advent of minimally invasive oesophagectomy

(MIO) over 15 years ago, debate has continued over

whether laparoscopic techniques are actually beneficial to

morbidity, and, further still, whether oncological resection

is compromised. This review article analyses the different

techniques employed in MIO and critically evaluates the

commonly reported outcome measures from available

literature.

Materials and methods

An electronic search for articles on the subject of laparo-

scopic oesophagectomy was performed through the Med-

line, Embase, Science Citation Index, Current Contents,

and PubMed databases. The search strategy involved

combining all of the available literature on the approach

(i.e., minimally invasive) with operation type (i.e., oeso-

phagectomy) for the disease process (i.e., oesophageal

cancer/neoplasm). Keywords used with respect to approach

were laparoscopy (MeSH terms, includes laparoscopic);

minimally AND invasive; minimally AND invasive AND

surgery (MeSH terms) OR operative OR procedures OR

operative procedures. Keywords used with respect to the

operation type were esophagectomy (MeSH term); oeso-

phagectomy (United Kingdom spelling). Keywords used

with respect to disease process were neoplasm (MeSH

terms); cancer. Further searches using keywords for oper-

ation subtypes (Ivor-Lewis; three-stage (o)esophagectomy;

transhiatal) did not reveal any further articles. Non-English

articles, articles pertaining only to benign processes, and

individual case reports were excluded. To date no ran-

domised controlled trials exist; the available literature is

limited to level III-2 evidence. All available case series and

reports on MIO for oesophageal cancer were included. The

minimally invasive techniques and reported data were

analysed, and from this a selection of commonly recogni-

sed outcome measures was generated. Following the defi-

nition of the important outcome measures, the studies were

separated into single-arm observational studies and com-

parative studies and also delineated by operative approach

and method of data collection (prospective versus retro-

spective). Data from case series with 15 or more patients

were included for data tabulation. Some overlap of data

was observed and was subsequently accounted for. Where

between-study homogeneity was clear, for example, mul-

tiple-case series reporting a purely minimally invasive

approach to both abdominal and thoracic components,

descriptive statistics were acquired using an electronic

statistics package (SPSS Statistics 17.0, SPSS Inc.). Using

the available data, we report the history of MIO, discuss

reported outcome measures, present thinking on current

best practice, and also postulate the future of oesophag-

ectomy. Where appropriate, comparisons were made with a

meta-analysis by Hulscher et al. [1] comparing open

transhiatal versus open transthoracic oesophagectomy.

Results

Thirty-one suitable articles [1], consisting of mainly pro-

spective and retrospective studies, were identified. Seven

series [25–31] directly compared open oesophagectomy

versus MIO; two of these [27, 28] were performed pro-

spectively. Review of 30 of the identified papers [2–31]

revealed three main groups of common outcome measures:

operative data, morbidity and mortality data, and onco-

logical resection data. Main operative outcome measures

were defined as total operative time, conversion rate, and

blood loss. Morbidity data was defined by early and late

complication rates, duration of intensive care requirement,

and total hospital stay. Complications of particular

importance were also recorded and comprised anastomotic

leaks, chylothorax, and specific respiratory morbidity.

Perioperative mortality was defined by death within

30 days from the procedure. Oncological outcome mea-

sures were pathological disease stage, margin involvement,

local recurrence, lymph node yield, and overall survival.

Neoadjuvant treatment numbers were included for each

study.

Twenty five case series containing 15 or more patients

were identified for data tabulation (Tables 1, 2, 3, 4, 5, 6, 7,

8). Operative time was recorded in 94% of the single-arm

observational studies and 86% of the comparative studies

(only one comparison study did not [27]). All 25 studies

included for data analysis reported important outcome

measures in percentages as follows: blood loss 81%, inci-

dence of anastomotic leak 68%, incidence of respiratory

morbidity 92%, incidence of chylothorax 96%, duration of

ICU stay 76%, duration of overall hospital stay 92%, 30-day

operative mortality 100%, extent of oncological resection

(positive margins/local recurrence and/or lymph node yield)

88%, survival at (variable) mean follow-up 72%.

Twelve case series [2–5, 8, 9, 13, 15, 25, 28, 29, 31]

directly reported results for completely minimally invasive

transthoracic oesophagectomy regardless of abdominal

component and anastomosis site. Selected results were as

follows (reported figures were weighted according to study

sample size, n is the number of studies included in the

calculation): mean operation time 312 min (range =

220–476 min) (n = 11); median blood loss 425 ml

Surg Endosc

123

(range = 65–700 ml) (n = 11); median incidence of

anastomotic leak 5.5% (range = 0–53.0%) (n = 9); med-

ian incidence of respiratory complications 31.7% (range =

0–223.5%) (n = 11); median incidence of chylothorax

5.2% (range = 2.2–26.7%) (n = 12); median duration of

ICU stay 1 day (range = 1–19 days) (n = 10); median

duration of hospital stay 13 days (range = 7–16 days)

(n = 12); median 30-day mortality 1.0% (range =

0–6.5%) (n = 12).

Nine case series [3, 5, 8, 13, 15, 25, 28, 29, 31] directly

reported results on a purely minimally invasive approach to

transthoracic oesophagectomy. Selected results from these

series were as follows: median operation time 330 min

(range = 220-413 min) (n = 9); median blood loss 279 ml

(range = 65–700 ml) (n = 9); median incidence of anas-

tomotic leak 5.6% (range = 0–40.0%) (n = 7); median

incidence of respiratory complications 7.8% (range =

3.1–60.0%) (n = 9); median incidence of chylothorax

3.0% (range = 1.0–4.0%) (n = 9); median duration of

ICU stay 1 day (range = 1–19 days) (n = 8); median dura-

tion of hospital stay 9 days (range = 7–14 days) (n = 9);

median 30-day mortality 1.0% (range = 0–3%) (n = 9).

Five case series [20–22, 24, 29] directly reported results

on a purely minimally invasive transhiatal technique.

Selected results from these series were as follows: mean

operation time 305 min (range = 200–415 min) (n = 5);

median blood loss 220 ml (range = 150–325 ml) (n = 4);

median incidence of anastomotic leak 8.0% (range =

7.7–29.2%) (n = 3); median incidence of respiratory

complications 9.0% (range = 8.3–25.0%) (n = 4); median

incidence of chylothorax 3.1% (range = 2.6–20.8%) (n =

5), median duration of ICU stay 1 day (range = 1–5 days)

(n = 3); median duration of hospital stay 12 days (ran-

ge = 7–17 days) (n = 5); median 30-day mortality 0%

(range = 0–4.6%) (n = 5).

Techniques of minimally invasive oesophagectomy

Two main techniques have been described for oesophageal

resection; transthoracic oesophagectomy and transhiatal

oesophagectomy. In total, three sites of exposure can be

utilised in oesophagectomy: the abdomen, the thorax, and

the neck. Transthoracic (Ivor-Lewis) resection involves

direct, and separate, abdominal and transthoracic access

Table 1 Operative data—single-centre cohort studies

Author/year Study

type

Patients

n (%)

Abdominal

component

Thoracic

component

Anastomosis

site

Operative

time (min)

Conversions

n (%)

Blood

loss

(ml)

Martin/05 [2] PST 36 Open or MI

(hand-assisted)

MI Cervical 263 2 200

Liebman/05 [3] PST 25 MI MI Cervical 330 2 (8) 300

Suzuki/05 [4] PST (not

stated)

19 MI (hand-assisted) MI Cervical 476 0 343

Palanivelu/06 [5] PST 130 MI MI Cervical 220 0 180

Bottger/06 [6] PST 25 MI—transhiatal,

3-stage

MI 12, open

4 (3-stage)

Cervical 165, 300 0 300

Godiris-Petit/06 [7] PST 25 MI Open Thoracic 368 1 (4) \100

Berrisford/08 [8] PST 77 MI MI Cervical 413 1 (1) 425

Robertson/95 [9] RST 17 Open MI Thoracic 330 5 (29) N/R

Kawahara/98 [11] RST 23 Open MI Cervical 111 (thoracic) 0 163

Nguyen/03 [13] RST 46 MI MI Both 350 2 279

Luketich/03 [14] RST 222 MI—transhiatal 8,

3-stage 214

MI Cervical N/R 16 (7.2) N/R

Collins/05 [15] RST 25 MI MI Cervical 350 2 200

Espat/04 [19] RST 15 MI—transhiatal

(robot-assisted)

N/A Cervical 274 0 50

Palanivelu/05 [20] PST 32 MI—transhiatal N/A None 200 0 150

Avital/05 [21] RST 22 MI—transhiatal N/A Cervical 380 1 (5) 220

Bann/05 [22] RST 20 MI—transhiatal N/A Cervical 415 2 (10) 300

Tinoco/07 [23] RST 78 MI—transhiatal N/A Cervical 153 (lap

component)

5 (6) N/R

Sanders/07 [24] RST 18 MI—transhiatal N/A Cervical 300 2 (11) N/R

MI minimally invasive, N/A not applicable, N/R not recorded, PST prospective series, RST retrospective series

Surg Endosc

123

with or without dissection at the cervical oesophagus

depending on the site of anastomosis. Transhiatal oeso-

phagectomy negates direct access to the mediastinum

through the thoracic wall and also may require dissection

of the cervical oesophagus depending on anastomosis site.

The first described techniques for MIO were in transhiatal

procedures by DePaula et al. [32] in Brazil and by Swan-

strom et al. [10] in North America. Subsequent to these,

video assistance was employed for transthoracic oeso-

phagectomy. As skills and technology have developed,

laparoscopy has become increasingly successful for the

abdominal component of Ivor-Lewis oesophageal resec-

tion. Gastric preconditioning, whereby the stomach is

mobilised on the right gastric arterial pedicle to assess

conduit viability prior to the resection surgery, is not

mentioned by the proponents of MIO.

Transhiatal oesophagectomy

As described, minimally invasive transhiatal oesophagec-

tomy was developed first and negates the need for trans-

thoracic exposure in an attempt to reduce postoperative

pulmonary complications. Most proponents of this proce-

dure use 5-port laparoscopy with the patient in varying

degrees of anti-Trendelenburg position. Although tech-

niques continue to be refined, most proponents describe

operator positioning between the patient’s legs, with the

camera holder and instrument nurse to the patient’s left

side and the second assistant to the right (Fig. 1). A con-

sensus on abdominal port placement is provided in Fig. 2.

All oncological oesophagectomies commence with a thor-

ough general inspection. The stomach may be mobilised

before or after oesophageal dissection. Irrespective of the

order, all lymph nodes and fatty tissue from the coeliac axis

and common hepatic and splenic arteries are cleared via an

incision through the lesser omentum; these are then swept

into the resection specimen. Oesophageal dissection begins

at the crura using harmonic shears with en bloc excision of

any locally involved tissue. The posterior mediastinum is

entered and adequate circumferential mobilisation of the

oesophagus is achieved by a combination of blunt and

sharp harmonic dissection. A tape may be passed around

the oesophagus to aid retraction, although some authors

[20] avoid this because of concern over tumour spill. A

proximal margin of at least 5 cm is the goal. The stomach

is mobilised in the usual fashion with preservation of the

right gastric artery and right gastroepiploic vascular arcade.

Although intrathoracic anastomosis has been described for

the transhiatal approach [29], this anastomosis site is

generally avoided with preference for a cervical anasto-

mosis following gastric pull-up. To achieve this, open

access and dissection are employed and the proximal

Table 2 Operative data—comparative series

Author/year Study type Patients

n (%)

Abdominal

component

Thoracic

component

Anastomosis

site

Operative

time

(min)

Conversion

n (%)

Blood

loss (ml)

Nguyen/00 [25] RST comparison 18 MI MI Cervical 364 0 297

16 Open Open Both 437 N/A 1046

20 Open—transhiatal None Cervical 391 N/A 1142

Bresadola/06 [26] RST comparison 14 MI—transhiatal,

thoracoscopic

Open Cervical 423 0 N/R

14 Open Open Cervical 359 N/A N/R

Braghetto/06 [27] PST comparison 60 (36.1) Open Cervical N/R N/A N/R

59 (35.5) Open—transhiatal None Cervical N/R N/A N/R

47 (22.3) MI MI Cervical N/R N/R N/R

Smithers/07 [28] PST comparison 23 MI MI Cervical 330 2 (9) 300

309 Open MI Cervical 300 10 (8.8) 600

114 Open Open Thoracic 285 N/A 400

Dapri/07 [29] RST comparison 24 MI—transhiatal None Both 300 0 325

15 MI MI Cervical 370 1 700

Fabian/07 [30] RST comparison 22 MI Both Both 333 1 (5) 178

43 Open Open Both 270 N/A 356

Fabian/08 [31] RST comparison 21 MI MI—prone Cervical 330 3 (9)—combined 65

11 MI MI—decubitus Cervical 375 3 (9)—combined 85

MI minimally invasive, N/A not applicable, N/R not recorded, PST prospective series, RST retrospective series

Surg Endosc

123

Table 3 Morbidity and mortality—single-centre cohort studies

Author/year Patients n Approach Early

complications

n (%)

Late

complications

n (%)

ICU stay

(days)

Hospital

stay (days)

30-day

mortality

n (%)

Martin/05 [2] 36 Transthoracic 15 (42) 1 (3) 1 16 2 (6)

Liebman/05 [3] 25 Transthoracic 16 (64) 1 (4) 19 11 0 (1 at 47 days)

Suzuki/05 [4] 19 Transthoracic 3 (16) 0 1 10 0

Palanivelu/06 [5] 130 Transthoracic 27 (20.8) 1 (0.8) 1 8 2 (1.5)

Bottger/06 [6] 25 Transthoracic 3 (12) 0 1.5 10 0

Godiris-Petit/06 [7] 25 Transthoracic 15 (60) 2 (8) 1 18 1 (4)

Berrisford/08 [8] 77 Transthoracic 33 (47) 3 (4) 6.5

(emergent only)

13 1 (1)

Robertson/95 [9] 17 Transthoracic 35 (207) 0 1 12 1 (6)

Kawahara/98 [11] 23 Transthoracic 9 (39) 1 (4) 0 26 0

Nguyen/03 [13] 46 Transthoracic (27) 0 2 8 (4)

Luketich/03 [14] 222 MI—transhiatal 8,

3-stage 214

124 (55.9) (27.3) 4 (1.8) 1 7 3 (1)

Collins/05 [15] 25 Transthoracic 20 (80) 1 (4) 1 9 1 (4)

Espat/04 [19] 15 Transhiatal

(robot-assisted)

N/R N/R 1 N/R 0

Palanivelu/05 [20] 32 Transhiatal 3 (9) N/R 1 7 0

Avital/05 [21] 22 Transhiatal 11 (50) 0 N/R 8 1 (5)

Bann/05 [22] 20 Transhiatal 15 (75) 0 1 17 0 (1 at 34 days)

Tinoco/07 [23] 78 Transhiatal 35 (45) 0 N/R 6.9 4 (6)

Sanders/07 [24] 18 Transhiatal 22 (122) 1 (6) N/R 15 0

Table 4 Morbidity and mortality—comparative studies

Author/year Patients

n (%)

Approach Early

complications

n (%)

Late

complications

n (%)

ICU stay

(days)

Hospital

stay

(days)

30-day

mortality

n (%)

Nguyen/00 [25] 18 MI 6 (33) 0–1 (6) chylous ascites 6.1 11.3 0

16 Open 8 (50) 0 9.9 23 0

20 Open—transhiatal 11 (55) 0 11.1 22.3 0 (1 at 70 days)

Bresadola/06 [26] 14 MI—transhiatal, thoracoscopic 5 (36) 3 (21) 3.4 16.4 0

14 Open 5 (36) 1 (7) 3.8 22.3 0

Braghetto/06 [27] 60 (36.1) Open 34 (57) 0 N/R N/R 7 (12)

59 (35.5) Open—transhiatal 33 (55) 0 N/R N/R 6 (10)

47 (22.3) MI 14 (30) 1 (13) N/R N/R 3 (6)

Smithers/07 [28] 23 MI 14 (61) N/R 1 11 0

114 Open and MI—thoracoscopic 193 (67) N/R 1 14 3 (2.6)

309 Open 76 (62) N/R 1 13 7 (2.3)

Dapri/07 [29] 24 Open—transhiatal 13 (54) 0 5 12 0

15 MI 13 (87) 0 5 14 0

Fabian/07 [30] 22 MI 15 (68) 0 N/R 9.5 1 (5)

43 Open 31 (72) 2 (5) N/R 11 4 (9)

11 MI 6 (55) 1 (9) N/R 9 0

Fabian 08 (31) 21 MI 10 (48) 0 N/R 10 1 (5)

11 MI 6 (55) 1 (9) N/R 9 0

Surg Endosc

123

oesophagus is divided using a linear stapler. After delivery

of the gastric conduit into the neck, cervical anastomosis is

achieved by either a hand-sewn interrupted technique or

stapler. In the event of any pleural breach, mediastinal

drains are placed, and prior to closure a feeding jejunos-

tomy is usually sited.

Transthoracic oesophagectomy

Minimally invasive transthoracic oesophagectomy involves

two or three stages depending on the site of oesophageal

anastomosis, and it has traditionally been felt that it offers

superior oncological resection when compared to the

transhiatal approach. Access to the abdomen and the cer-

vical area is generally achieved with the patient in the anti-

Trendelenburg position, whereas thoracoscopic access is

better with the lateral or prone position. Because of the

subsequent need for intraoperative repositioning, the order

by which the transthoracic technique is achieved tends to

depend on the site of anastomosis. For intrathoracic anas-

tomosis, it seems logical to fully complete the abdominal

component of the operation prior to repositioning for

thoracoscopic dissection and anastomosis, thus avoiding

the need for further unnecessary movement of the patient.

Likewise, in the situation of cervical anastomosis, com-

pleting the thoracoscopic dissection prior to the abdominal

and cervical components achieves the same economy of

movement.

Where cervical anastomosis is to be performed, the first

stage of the operation varies among authors; some prefer

initial dissection in the abdomen, whilst others prefer initial

oesophageal mobilisation in the thorax. As described

above, the latter approach reduces the required amount of

intraoperative repositioning. Irrespective of this, the

abdominal component of the procedure proceeds in a fairly

universal way. The anti-Trendelenburg position is acquired

and a 5-port laparoscopy is set up, not dissimilar in pattern

to that of the transhiatal procedure described above

(Figs. 1, 2); however, the operator usually stands on the

patient’s right side instead of between the legs. The pri-

mary assistant stands on the patient’s left with the monitor

placed at the patient’s head end. Stomach is most com-

monly used for conduit, but colon may be required in the

situation of distal tumour spread or previous gastrectomy.

Table 5 Complications—single-centre cohort studies

Author/year Patients n Approach Anastomotic

leaks n (%)

Respiratory

complications

n (%)

Specific respiratory

complications

Chylothorax

n (%)

Martin/05 [2] 36 Transthoracic 2 (6) 2 (6) Pneumonia, ARDS 7 (19)

Liebman/05 [3] 25 Transthoracic 0 15 (60) Pneumonia, pleural effusion,

atelectasis, pneumonthorax

2 (8)

Suzuki/05 [4] 19 Transthoracic 1 (5) 0 N/A 1 (5)

Palanivelu/06 [5] 130 Transthoracic N/R 4 (3) Pneumonia, ards, pleural effusion 3 (2.3)

Bottger/06 [6] 25 Transthoracic 2 (8) 1 (11) Gastric-bronchial fistula 3 (12)

Godiris-Petit/06 [7] 25 Transthoracic N/R 11 (44) Pneumoia, ARDS, pneumothorax,

pleuritis

2 (8)

Berrisford/08 [8] 77 Transthoracic N/R 6 (9) Pneumonia, respiratory failure 3 (4)

Robertson/95 [9] 17 Transthoracic 9 (53) 38 (224) Pneumonia, pneumothorax, pleural

effusion, empyema

3 (18)

Kawahara/98 [11] 23 Transthoracic N/R 2 (9) Pneumonia 1 (4)

Nguyen/03 [13] 46 Transthoracic 2 (4) 4 (9) Pneumonia, pleural effusion,

gastric-tracheal fistula

1 (2)

Luketich/03 [14] 222 Transthoracic 214,

transhiatal 8

26 (11.7) 45 (20.3) Pneumonia, ARDS, pleural

effusion, atelectasis

7 (3.2)

Collins/05 [15] 25 Transthoracic 6 (24) 8 (32) Pneumonia, atelectasis, pleural

effusion, empyema

3 (12)

Espat/04 [19] 15 Transhiatal

(Robot-assisted)

N/R N/R N/A N/R

Palanivelu/05 [20] 32 Transhiatal N/R N/R N/A 1 (3)

Avital/05 [21] 22 Transhiatal 3 (14) 5 (23) Pneumonia, atelectasis 1 (5)

Bann/05 [22] 20 Transhiatal N/R 5 (25) Pneumonia, atelectasis 2 (10)

Tinoco/07 [23] 78 Transhiatal 10 (13) 14 (18) Pneumonia, pleural effusion,

pneumothorax, empyema

10 (13)

Sanders/07 [24] 18 Transhiatal 6 (33) 7 (39) Pneumonia, atelectasis 2 (11)

Surg Endosc

123

For gastric conduit, mobilisation of the stomach is per-

formed as per the transhiatal approach. Kocherisation of

the duodenum is required to mobilise the pylorus to the

oesophageal hiatus. Dissection of the lower oesophagus

can be achieved as far as the extent of direct vision. The

gastric conduit is created using multiple loads of a linear

cutting stapler, starting at the lesser curvature. Many

operators do not complete transection of the pathologic

specimen at this point as keeping this continuity later

facilitates retraction of the conduit into the chest.

The thoracic component is performed with the patient in

either a lateral or a prone position (Figs. 3, 4) to aid

exposure of the mediastinal oesophagus. The prone posi-

tion, in particular, places the oesophagus at the upper limit

in the thorax and enables the right lung to fall away under

gravity [12]. The clear disadvantages of the prone tech-

nique are the inherent practical issues of physically

achieving such a position and the associated difficulty with

airway management. There is little consensus on thoracic

port placements, which are dependent on patient position-

ing. Single-lung ventilation is required. Where patients

have not tolerated single-lung ventilation, low-pressure gas

insufflation has been successfully employed. Dissection is

achieved with ultrasonic shears, and manipulation of the

oesophagus is aided by looping tape around its circum-

ference from an early stage.

Following oesophageal mobilisation, the specimen can

be manipulated and transected in the thorax, abdomen, or

neck depending on disease site and surgeon’s preference.

Anastomosis sites and technique vary among authors.

When an intrathoracic anastomosis is required, technique is

particularly critical to reduce the risk of leak and its

associated morbidity. All minimally invasive techniques

for intrathoracic anastomosis describe use of a circular end-

to-end stapler. The detachable anvil may be introduced into

the proximal oesophagus via either abdomen or thorax, but

extension of thoracic port sites is avoided where possible.

Following ligature or clamp occlusion of the proximal

margin of the specimen, the anvil is introduced into the

proximal oesophagus via a transverse incision. Anvil

anchorage is now necessary and has been regarded as a

rate-limiting step. Two principal methods of anvil fixation

are subsequently described: purse string and ligature

techniques. The traditional method of purse string

placement is time consuming in MIO and has led to the

development of new instruments and techniques. The

Endo-Stitch device (US Surgical), described by Misawa

et al. [33], consists of a two-jawed endoscopic instrument

with each jaw capable of holding a double-ended straight

needle. Used on soft tissues, this instrument enables the

placement of running or interrupted sutures more effi-

ciently by one hand. The alternative Z-stitch technique,

Table 6 Complications—comparative studies

Authors Patients

n (%)

Approach Anastomotic

leaks n (%)

Respiratory

complications

n (%)

Specific respiratory

complications

Chylothorax

n (%)

Nguyen/00 [25] 18 MI 1 (6) 3 (17) Gastric-bronchial fistula,

respiratory failure

2 (11)

16 Open 0 3 (19) Respiratory failure 2 (12)

20 Open—transhiatal 0 3 (15) Respiratory failure 2 (10)

Bresadola/06 [26] 14 MI—transhiatal, thoracoscopic 2 (14) 1 (7) Respiratory failure 0

14 Open 1 (7) 2 (14) Respiratory failure 0

Braghetto/06 [27] 60 (36.1) Open 37 (62) 17 (28) Pneumonia, pleural effusion 13 (22)

59 (35.5) Open—transhiatal 35 (59) 18 (31) Pneumonia, pleural effusion 13 (22)

47 (22.3) MI 18 (38) 9 (19) Pneumonia, pleural effusion 4 (9)

Smithers/07 [28] 23 MI 4 (17) 8 (34) Pneumonia, pleural effusion 1 (4)

309 Open and MI—thoracoscopic 17 (5.5) 98 (31.7) Pneumonia, pleural effusion 16 (5)

114 Open 10 (8.7) 44 (38.6) Pneumonia, pleural effusion 7 (6.1)

Dapri/07 [29] 24 Open—transhiatal (29) 2 (8) Pneumonia, pneumothorax 5 (28)

15 MI 6 (40) 1 (7) Respiratory failure 4 (27)

Fabian/07 [30] 22 MI 1 (5) 6 (27) Respiratory failure, pneumonia,

reintubation

3 (14)

43 Open 2 (5) 41 (95) Respiratory failure, pneumonia,

reintubation

3 (7)

Fabian/08 [31] 21 MI N/R 3 (12) Pneumonia, respiratory failure 1 (4)

11 MI N/R 2 (18) Pneumonia, respiratory failure 2 (18)

Surg Endosc

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Table 7 Oncological data—single-centre series

Author/year Patients

n (%)

Approach Pathological

tumour stage

Neoadjuvant

therapy n (%)

Positive margins/

local recurrence

n (%)

Lymph

nodes

Survival (%)

(follow-up period)

Martin/05 [2] 36 Transthoracic II–IV 23 (68) 5 (14)/N/R N/R 44 (4 yr)

Liebman/05 [3] 25 Transthoracic 0–III 8 (32) 4 (16)/4 (16) 17 32 mo (32 mo)

Suzuki/05 [4] 19 Transthoracic 0–Iva 5 (26) 0/0 N/R N/R

Palanivelu/06 [5] 130 Transthoracic I–III 1 (0.8) N/R 18 75–18 (20 mo)

Bottger/06 [6] 25 Transthoracic I–III N/R N/R (all tumours

lower 1/3)

14, 23a N/R

Godiris-Petit/06 [7] 25 Transthoracic 0–IV 5 (20) 0/2 (4) 12 56 (2 yr)

Berrisford/08 [8] 77 Transthoracic 0–IV 44 (68) 2 (3)/3 (4) 21 81 (2 yr)

Robertson/95 [9] 17 Transthoracic II–III 0 2 (12)/5 (29) 7 59 (23 mo)

Kawahara/98 [11] 23 Transthoracic 0–IV 5 (28) 0/1 (4) 29 78 (15 mo)

Nguyen/03 [13] 46 Transthoracic I–IV 23 (61) 0/N/R 10 57

Luketich/03 [14] 222 MI—transhiatal 8, 3-stage 214 0–III 36 (16) N/R N/R 20–95 (19 mo)

Collins/05 [15] 25 Transthoracic 0–IV 7 (28) 1 (4)/N/R 9 N/R

Espat/04 [19] 15 Transhiatal (robot-assisted) II–III 0 0/1 (3) 19 67 (27 mo)

Palanivelu/05 [20] 32 Transhiatal N/R N/R 0/N/R N/R N/R

Avital/05 [21] 22 Transhiatal I–III N/R N/R 14 61

Bann/05 [22] 20 Transhiatal N/R 0 0/0 5 84 (11 mo)

Tinoco/07 [23] 78 Transhiatal I–IV N/R N/R N/R 19 (4 yr)

Sanders/07 [24] 18 Transhiatal I–III 1 (6) N/R 10 72 (13 mo)

a Study included 12 Pure MI Transhiatal resections, 14 lymph node harvest, and 4 Three-Stage resections with open thoracic component, 23

lymph node harvest

Table 8 Oncological data—comparative series

Authors Patients

n (%)

Approach Pathological

tumour stage

Neoadjuvant

therapy n (%)

Positive margins/

local recurrence

n (%)

Lymph

nodes

Survival (%)

(follow-up period)

Nguyen/00 [25] 18 MI N/R N/R 0/0 11 100 (3 mo)

16 Open N/R N/R 1 (6) 6 N/R

20 Open—transhiatal N/R N/R 1 (5) 7 N/R

Bresadola/06 [26] 14 MI—transhiatal, thoracoscopic I-III N/R N/R 22 N/R

14 Open I-IV N/R N/R 19 N/R

Braghetto/06 [27] 60 (36.1) Open I-III N/R N/R N/R 34

59 (35.5) Open—transhiatal N/R N/R N/R N/R 33

47 (22.3) MI N/R N/R N/R N/R 46

Smithers/07 [28] 23 MI I-III N/R 5 (20)/N/R 17 22 (5 yr)

114 Open and MI—thoracoscopic 0-IV N/R 21 (14)/N/R 16 41 (5 yr)

309 Open 0-IV N/R 42 (19)/N/R 17 16 (5 yr)

Dapri/07 [29] 24 Open—Transhiatal I-IV 2 (8) 0/N/R 3 50

15 MI is-III 2 (13) 0/N/R 4 47

Fabian/07 [30] 22 MI is-IV 9 (4.1) 0/N/R 15 N/R

43 Open is-IV 16 (37) 3 (6)/N/R 8 N/R

Fabian/08 [31] 21 MI is-III 9 (43) 0/N/R 15.5 N/R

11 MI is-III 3 (27) 0/N/R 14.6 N/R

Surg Endosc

123

described by Thairu [34], utilises cross-firing of a linear

stapler to create a 60� angle at the proximal oesophagus

whilst the anvil is in situ. The smaller aperture associated

with this technique enables a Z-stitch to suffice for

anchorage. The ligature technique applies a principle first

reported by Allsop [35] in colorectal anastomoses and is

described by Lee [36] in the setting of oesophagectomy.

This method avoids purse string creation altogether by

single ligature approximation of the oesophagus onto the

purse string notch of the anvil. Once anvil placement and

anchorage are achieved, the final specimen resection and

oesophagogastric anastomosis are performed in a uniform

manner. The specimen is delivered into the abdomen and

divided distally with a linear stapler. Distal transverse

gastrotomy enables introduction of the proximal circular

stapler, which is then carefully advanced in a caudal

direction until correctly positioned within the tubularised

stomach and in apposition to the proximal oesophagus. The

anvil and stapler are engaged and the anastomosis com-

pleted. A pleurally sited intercostal catheter can be placed

for drainage.

Discussion

Open oesophagectomy utilising a transthoracic or transhi-

atal approach remains the gold standard treatment for

benign and malignant conditions of the oesophagus. Both

of these open approaches to oesophageal resection have

been validated and a recent meta-analysis [1] suggests that

Fig. 1 General operating room layout for the laparoscopic abdominal

component of MIO. An, anaesthetist; Ass 1, assistant 1; Ass 2,

assistant 2; IN, instrument nurse; M, monitor; S, surgeon

Fig. 2 Laparoscopic port site placement for abdominal part of MIO.

A, C, D 5-mm ports. B 10-mm port

Fig. 3 Thoracoscopic port site placement for MIO: left lateral

decubitus position. A, B 5-mm ports. C, D 10-mm ports

Fig. 4 Thoracoscopic port site placement for MIO: prone position. A,

C 5-mm ports. B 10-mm port

Surg Endosc

123

they result in similar morbidity, mortality, and 5-year

survival rates. Theoretically, respiratory morbidity should

occur more frequently in the transthoracic approach but no

statistically significant difference has been shown.

No randomised controlled trials currently exist for MIO,

and it seems unlikely that any will be carried out given the

known limitations of the procedure for locally advanced

primary disease. This, in addition to the high dependence

of MIO on advanced technical skill, has resulted in a slow

acceptance of this technique as a valid or achievable

standard of care. The available comparative data do sug-

gest that MIO is as good as open oesophagectomy when

performed by an appropriately skilled and experienced

surgeon. Of particular note is the work of Luketich et al.

[14, 37], who have reported the largest series of MIO (222

patients), albeit noncomparatively. Morbidity rates are at

least comparable to open procedures in this series. Luke-

tich’s mortality rate of 1.3% is better than the mortality rate

of 5.7% for transhiatal oesophagectomy (THO) and 9.2%

for transthoracic oesophagectomy (TTO) reported in the

meta-analysis by Hulscher et al. [1] on open oesophagec-

tomy. It is generally accepted that outcome following open

oesophagectomy is better when performed in high numbers

by dedicated surgeons, and it is logical to extrapolate that

theory for MIO. Even so, MIO has been reported by

smaller centres with comparable outcome measures to open

oesophagectomy. For example, Bann et al. [22] reported on

a prospective series of 22 patients who underwent Ivor-

Lewis MIO at a district general hospital in the United

Kingdom with oncological resection and morbidity results

comparable to those of open oesophagectomy. Review of

the existing studies shows a number of commonly assessed

outcome measures for morbidity and oncological resection

which will now be addressed individually.

Operative data

Operative time

It is unanimously accepted that total operative time

(Tables 1, 2) is longer for MIO than for open surgery and

except for the limitation caused by local oncological stage,

this remains the major drawback in MIO. As with all

comparisons to open oesophagectomy, variability in study

size and subsequently induced statistical error need to be

considered, as does the inherent selection bias of patients

more likely to have less advanced and therefore more

easily resectable disease.

Blood loss

Blood loss is reported by most authors in this series, with

the range of averages between 50 and 700 ml (Tables 1, 2).

The study with the lowest blood loss was by Espat [19] in

2004, who used a robot-assisted transhiatal approach in 15

patients with no conversions. There are no other recorded

studies using this technology in the literature, which is not

surprising given that robot-assisted surgery still remains

very much in the avant-garde and is inaccessible to the vast

majority of institutions. Otherwise little solid comparative

data to open surgery exists, but there is certainly no

overwhelming evidence of any significant difference in

haemorrhage between MIO and open oesophagectomy.

Morbidity and mortality

Anastomotic leakage

Anastomotic leak is one of the most feared complications

in oesophagectomy surgery, with a historical mortality rate

of 50%. The definition of anastomotic leak varies between

authors although most in this series used radiographic

findings, whether carried out as a routine or because of

clinical suspicion. From our analysis, MIO leakage rate

ranged between 2.2 and 52.9% (Tables 5, 6), which is at

least comparable to the reported leakage rates for open

oesophagectomy [1], where rates vary from 3 to 50%. The

wide range of leakage rate reported following open oeso-

phagectomy was addressed by Hulscher et al. [1] in their

meta-analysis, and they concluded that this wide-ranging

result was more a reflection of the problem with definition

rather than true technical differences. There is no apparent

difference between leakage rates in thoracic or cervical

anastomosis following MIO. For open surgery, transhiatal

operations with cervical anastomoses seem to produce

almost twice the anastomotic leak compared to transtho-

racic operations, where a majority of anastomoses were

made through the chest (13.6 vs. 7.2%) [1]. From our

collated data this does not appear to be reflected in MIO.

Irrespective of absolute leakage rate, thoracic leakage tends

to result in higher morbidity than cervical leakage, and this

should be considered in addition to absolute numbers.

Respiratory morbidity

Major morbidity results from open transthoracic access.

The thoracotomy incision is painful and also exposes the

lungs to atmospheric pressure for extended periods,

increasing barotrauma risk. Open transhiatal techniques

were first developed in an attempt to avoid thoracotomy,

but the inherent element of blind resection in this technique

raised some concern over the adequacy of oncological

resection and led to the first minimally invasive thoraco-

scopic approaches. Analysis of respiratory complication

rate, however, shows fairly underwhelming results when

compared to open techniques. Analysis of the 12 case

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123

series that report results on a transthoracic approach [2–5,

8, 9, 13, 15, 25, 28, 29, 31] provides a weighted median

respiratory complication rate of 31.7%, which is high

compared to the published data on open oesophagectomy;

the meta-analysis by Hulcher et al. [1] reports respiratory

complication rates of 18.7% for open transthoracic surgery

and 12.7% for open transhiatal oesophagectomy. This

alarming result is, however, probably more reflective of

variation in reporting than a true difference. The notable

extreme in respiratory complication rate was observed in

the retrospective review of 17 patients who underwent a

two-stage oesophagectomy performed by Robertson et al.

[9]. In this series radiographic evidence of atelectasis was

included in the complication rate irrespective of the clinical

picture and thus accounted for 76% of all patients alone.

Analysis of the available series that reported results of a

purely minimally invasive approach to both the abdominal

and the thoracic component reveals more promising

information, with a combined respiratory complication rate

of 7.8%. The largest available series by Luketich [14] was

not included in either of the above grouped case series

because 8 of 222 patients underwent transhiatal oeso-

phagectomy and could not be differentiated from the

remaining 214. This series reports a 12.6% combined

respiratory complication rate defined as pneumonia and/or

acute respiratory distress syndrome (ARDS). Meta-analysis

of the open technique by Hulscher et al. [1] grouped pul-

monary complications together, including pulmonary

embolus (PE) with pneumonia and ARDS. The addition of

PE to the Luketich et al. [14] data results in a morbidity

rate of 14% compared to 18.7% for open transthoracic and

12.7% for open transthoracic techniques. It should be noted

that Luketich et al. preferred the improved access of a

minimally invasive transthoracic approach and that their

morbidity result is at least comparable to that of the open

transhiatal technique but with the benefits of improved

mediastinal exposure.

Postoperative intensive care requirements

and hospital stay

Median duration of postoperative stay on the intensive care

unit (ICU) following MIO is 1 day in the majority of studies

(Tables 3, 4). Some postoperative care protocols following

MIO did not involve planned admission to ICU at all. In a

series of 77 patients who underwent minimally invasive

transthoracic oesophagectomy, Berrisford et al. [8] used

ward-based postoperative care with central venous moni-

toring. This approach resulted in a 14% emergency admis-

sion rate to the formal ICU, however, and median stay on the

ICU in these patients was longer at 6.5 days. It remains to be

proven whether the avoidance of routine admission to ICU

following MIO is a safe or cost-effective practice.

Mortality

Thirty-day mortality rates following MIO vary between 0

to 5.9% (Tables 3, 4), which compares to the open trans-

thoracic procedure mortality rate of 9.2% and open trans-

hiatal procedure mortality rate of 7.2% described by

Hulscher et al. [1] in their meta-analysis. Patient selection

for surgery may well bias these results, but most propo-

nents of MIO believe this technique to be superior to open

surgery in patients with early disease.

Oncological resection

Since the advent of MIO, the adequacy of oncological

resection compared to that of open surgery has been

questioned. Important and commonly reported outcome

measures are resection margins, lymph node numbers,

overall disease stage, and long-term survival.

All potentially curative oncological resections require

complete clearance of local disease and therefore clear

resection margins (i.e., R0) of the primary tumour are

subsequently of the utmost importance. During the initial

development of MIO, only benign or early-stage malignant

disease was considered, and for most proponents of MIO

this still remains the case. This practice is based on the

expert opinion of these surgeons that an open approach still

provides better oncological clearance for locally advanced

disease compared to MIO and that potential cure from this

outweighs the known difference in morbidity risk. The

range of final pathological stage following MIO for

malignant disease does range from 0 to IV (Tables 7, 8).

Where a pathological stage IV was reported, surgery was

usually completed on palliative grounds or when previ-

ously undiagnosed metastatic spread could be concomi-

tantly resected. It should also be remembered that stage

migration [38] can bias analysis of pathological stage. This

upstaging is based on the idea that a more extensive lym-

phatic dissection results in a higher probability of node

positive disease being diagnosed. Stage migration will also

result in a more favourable long-term outcome relative to

pathological stage.

Where reported, MIO results in clear resection margins

in the vast majority. Martin et al. [2] reported the highest

rate of resection margin involvement in a study of 36

patients who underwent hybrid three-stage transthoracic

oesophagectomy. The technique included thoracoscopic

mobilisation of the mediastinal oesophagus and hand-

assisted laparoscopy in 21 patients and open laparotomy in

the remaining 15. Of all resections, five had involved

margins. Two were found to have unresectable primary

disease irrespective of approach and three had positive

radial margins, none of whom had received neoadjuvant

therapy. On this note, at least one study [11] revealed an

Surg Endosc

123

excellent response of some tumours to neoadjuvant therapy

with significant pathological downstaging and subsequent

successful resection with minimally invasive techniques.

Even with open oesophagectomy, there is still debate as

to the best approach for optimal lymph node dissection.

Given this, we will not comment on comparative data

between transhiatal and transthoracic minimally invasive

techniques. Analysis of all articles that used minimally

invasive techniques on ten or more patients provides a

range of average lymph nodes sampled of between 5 and

29 (Tables 7, 8). Variations on the extent of lymphatic

dissection for any approach to oesophagectomy do exist

and will undoubtedly bias the quoted figures influencing

overall staging via stage migration.

Survival

Long-term survival following MIO varies. This is largely

due to the retrospective data collection in most of the

existing studies. If reliable 3- and 5-year survival follow-up

data were available, one would expect similar results

compared to stage-equivalent patients who underwent open

surgery where clear margins and ‘‘adequate’’ lymphatic

clearance were achieved, but this is speculative.

Learning curve/progression

The best example of progression in MIO comes from

Luketich et al. [14, 37], who have published serial data on

their experience. The initial approach was with laparo-

scopic transhiatal oesophagectomy, which changed to a

thoracoscopic transhiatal technique over time. The initial

description was of 77 patients who underwent MIO

between August 1996 and September 1999 [37]. This has

now been extended to include data for a total of 222

patients [14], the largest single series of any experience

with MIO. Median operative time for the first 20 cases was

450 min, which decreased to 270 min thereafter. Anasto-

motic leak rate from initial experience was 9%, which

increased slightly to 11.7% over all 222 patients. As

experience grew, the minor complication rate decreased

and the major complication rate increased. Overall mor-

tality rate for the 222 patients was 1.4%. Progressively

more advanced disease has become amenable to MIO

through this series and should be taken into account when

considering these data.

Conclusions

For benign disease and oesophageal cancer of stage III or

less, MIO appears to be at least as good as open techniques

when performed by experienced surgeons in large centres.

Trends show acceptable morbidity, improved postoperative

recovery time, and adequate oncological resection for early

malignant disease. The immediately obvious negative

aspects of MIO are the experience requirement, the need

for advanced minimally invasive skills and equipment, and

the increased operative time. Morbidity following tho-

racoscopic and transhiatal MIO techniques is similar.

Whilst the transhiatal approach requires less intraoperative

positioning, access to the mediastinum via the hiatus is

limited and may compromise the extent of oncological

resection. Thoracoscopy provides improved exposure to

the middle and upper oesophagus and thoracic lymph

nodes. Although the oncological outcome data following

transhiatal MIO is scarce and negates further objective

comparison to the thoracoscopic technique, achieving long-

term locoregional control is the primary goal in any cancer

surgery. For this reason, thoracoscopic mobilisation of the

oesophagus, with either an open or a laparoscopic

abdominal component, is the currently preferred technique

for most surgeons. It is still felt that locally advanced

disease is a strong contraindication to MIO, irrespective of

approach. There will always be an inherent conversion rate

for intraoperative complications, such as uncontrolled

haemorrhage, and patient factors, such as adhesions. Where

this occurs, morbidity arguably may be higher than with a

primary open procedure. There remains no level I evidence

on which to draw firmer conclusions and it is unlikely that

a multicentre randomised controlled trial will come to

fruition. In the eyes of proponents of MIO, this may be

irrelevant. When used for carefully selected patients with

benign disease or early cancer, data from the literature does

show that MIO can result in superior outcome measures

and is at least comparable to open resection in this group.

Disclosures Nick Butler, Stuart Collins, Breda Memon, and Mu-

hammed Ashraf Memon have no conflicts of interest or financial ties

to disclose.

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